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An omics-based framework for assessing the health risk of antimicrobial resistance genes

Author

Listed:
  • An-Ni Zhang

    (The University of Hong Kong
    Massachusetts Institute of Technology)

  • Jeffry M. Gaston

    (Google)

  • Chengzhen L. Dai

    (Massachusetts Institute of Technology)

  • Shijie Zhao

    (Massachusetts Institute of Technology)

  • Mathilde Poyet

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    The Broad Institute of MIT and Harvard)

  • Mathieu Groussin

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    The Broad Institute of MIT and Harvard)

  • Xiaole Yin

    (The University of Hong Kong)

  • Li-Guan Li

    (The University of Hong Kong)

  • Mark C. M. Loosdrecht

    (Delft University of Technology)

  • Edward Topp

    (Agriculture and Agri-Food Canada)

  • Michael R. Gillings

    (Macquarie University)

  • William P. Hanage

    (Harvard TH Chan School of Public Health)

  • James M. Tiedje

    (Michigan State University)

  • Katya Moniz

    (Massachusetts Institute of Technology)

  • Eric J. Alm

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    The Broad Institute of MIT and Harvard)

  • Tong Zhang

    (The University of Hong Kong
    The University of Hong Kong
    The University of Hong Kong)

Abstract

Antibiotic resistance genes (ARGs) are widespread among bacteria. However, not all ARGs pose serious threats to public health, highlighting the importance of identifying those that are high-risk. Here, we developed an ‘omics-based’ framework to evaluate ARG risk considering human-associated-enrichment, gene mobility, and host pathogenicity. Our framework classifies human-associated, mobile ARGs (3.6% of all ARGs) as the highest risk, which we further differentiate as ‘current threats’ (Rank I; 3%) - already present among pathogens - and ‘future threats’ (Rank II; 0.6%) - novel resistance emerging from non-pathogens. Our framework identified 73 ‘current threat’ ARG families. Of these, 35 were among the 37 high-risk ARGs proposed by the World Health Organization and other literature; the remaining 38 were significantly enriched in hospital plasmids. By evaluating all pathogen genomes released since framework construction, we confirmed that ARGs that recently transferred into pathogens were significantly enriched in Rank II (‘future threats’). Lastly, we applied the framework to gut microbiome genomes from fecal microbiota transplantation donors. We found that although ARGs were widespread (73% of genomes), only 8.9% of genomes contained high-risk ARGs. Our framework provides an easy-to-implement approach to identify current and future antimicrobial resistance threats, with potential clinical applications including reducing risk of microbiome-based interventions.

Suggested Citation

  • An-Ni Zhang & Jeffry M. Gaston & Chengzhen L. Dai & Shijie Zhao & Mathilde Poyet & Mathieu Groussin & Xiaole Yin & Li-Guan Li & Mark C. M. Loosdrecht & Edward Topp & Michael R. Gillings & William P. H, 2021. "An omics-based framework for assessing the health risk of antimicrobial resistance genes," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-25096-3
    DOI: 10.1038/s41467-021-25096-3
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    Cited by:

    1. Achal Dhariwal & Polona Rajar & Gabriela Salvadori & Heidi Aarø Åmdal & Dag Berild & Ola Didrik Saugstad & Drude Fugelseth & Gorm Greisen & Ulf Dahle & Kirsti Haaland & Fernanda Cristina Petersen, 2024. "Prolonged hospitalization signature and early antibiotic effects on the nasopharyngeal resistome in preterm infants," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Yi-Fei Wang & Yan-Jie Liu & Yan-Mei Fu & Jia-Yang Xu & Tian-Lun Zhang & Hui-Ling Cui & Min Qiao & Matthias C. Rillig & Yong-Guan Zhu & Dong Zhu, 2024. "Microplastic diversity increases the abundance of antibiotic resistance genes in soil," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Zhenyan Zhang & Qi Zhang & Tingzhang Wang & Nuohan Xu & Tao Lu & Wenjie Hong & Josep Penuelas & Michael Gillings & Meixia Wang & Wenwen Gao & Haifeng Qian, 2022. "Assessment of global health risk of antibiotic resistance genes," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    4. Zi-Teng Liu & Rui-Ao Ma & Dong Zhu & Konstantinos T. Konstantinidis & Yong-Guan Zhu & Si-Yu Zhang, 2024. "Organic fertilization co-selects genetically linked antibiotic and metal(loid) resistance genes in global soil microbiome," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    5. Michelle Baker & Xibin Zhang & Alexandre Maciel-Guerra & Kubra Babaarslan & Yinping Dong & Wei Wang & Yujie Hu & David Renney & Longhai Liu & Hui Li & Maqsud Hossain & Stephan Heeb & Zhiqin Tong & Nic, 2024. "Convergence of resistance and evolutionary responses in Escherichia coli and Salmonella enterica co-inhabiting chicken farms in China," Nature Communications, Nature, vol. 15(1), pages 1-21, December.

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